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Sequence Composition and Genome Organization of Maize

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Sequence Composition and Genome Organization of Maize Sequence composition and genome organization of maize Joachim Messing*†, Arvind K. Bharti*, Wojciech M. Karlowski‡, Heidrun Gundlach‡, Hye Ran Kim§, Yeisoo Yu§, Fusheng Wei§, Galina Fuks*, Carol A. Soderlund¶, Klaus F. X. Mayer‡, and Rod A. Wing§ *Plant Genome Initiative at Rutgers, Waksman Institute, Rutgers, The State University of New Jersey, Piscataway, NJ 08854; ‡Munich Information Center for Protein Sequences, Institute for Bioinformatics, GSF Research Center for Environment and Health, D-85764 Neuherberg, Germany; and §Arizona Genomics Institute and ¶Arizona Genomics Computational Laboratory, University of Arizona, Tucson, AZ 85721 Communicated by Brian A. Larkins, University of Arizona, Tucson, AZ, August 20, 2004 (received for review July 22, 2004) Zea mays L. ssp. mays, or corn, one of the most important crops and regions was performed with DNA markers (7) and by comparative a model for plant genetics, has a genome Ϸ80% the size of the mapping to close relatives of maize (8, 9). human genome. To gain global insight into the organization of its Although genetic and cytogenetic analyses provided us with a genome, we have sequenced the ends of large insert clones, global view of the organization of the maize genome, a more yielding a cumulative length of one-eighth of the genome with a detailed analysis will come from its DNA sequence. In fact, the DNA sequence read every 6.2 kb, thereby describing a large maize genome is most likely the next plant genome that will be percentage of the genes and transposable elements of maize in an sequenced after Arabidopsis and rice. However, because of its unbiased approach. Based on the accumulative 307 Mb of se- suspected greater sequence complexity than the human genome, quence, repeat sequences occupy 58% and genic regions occupy maize is also thought to be the next technical challenge in genome 7.5%. A conservative estimate predicts Ϸ59,000 genes, which is sequencing. When large genomes are dissected into overlapping higher than in any other organism sequenced so far. Because the bacterial artificial chromosome (BAC) clones, these clones can be sequences are derived from bacterial artificial chromosome clones, assembled into megabase (Mb)-sized chromosomal fragments which are ordered in overlapping bins, tagged genes are also through fingerprinting methods. After the fragments are assigned ordered along continuous chromosomal segments. Based on this to their chromosomal locations, sequences from the BAC clones positional information, roughly one-third of the genes appear to become positioned relative to the genetic map, thereby serving as consist of tandemly arrayed gene families. Although the ancestor anchors for other sequences. of maize arose by tetraploidization, fewer than half of the genes Following this concept, we have generated Ϸ475,000 maize BAC appear to be present in two orthologous copies, indicating that the end sequences (BESs) with a cumulative length of 307 Mb, pro- maize genome has undergone significant gene loss since the viding an 8-fold coverage of the genome. BES reads averaged 647 duplication event. bp with an average distribution of one end every 6.2 kb of the genome. Besides constituting a framework for sequencing the maize genome ͉ whole-genome sequence tags ͉ map-based sequence ͉ maize genome, the BES provided us with a comprehensive, quan- whole-genome duplication ͉ gene families titative data set, which allowed us to assess maize transposable element (TE) and gene content. Moreover, by examining the lant genomes differ from mammalian genomes by their enor- physical linkage of BESs, we determined that a large proportion of Pmous range in size. Whereas mammalian genomes range be- the maize gene set consists of tandemly arrayed gene families, and tween 2 and 3 gigabases (Gb), the major crop plants vary from 0.4 that a heavy loss of unlinked duplicated genes must have occurred Gb in rice to 16 Gb in wheat. The model plant Arabidopsis has an during the transition from a tetraploid to a diploid species. even smaller genome of 0.125 Gb and was, therefore, the first plant SCIENCES Materials and Methods to be sequenced in its entirety (1). The only other plant genome that AGRICULTURAL has been sequenced is from rice (http:͞͞rgp.dna.affrc.go.jp). Ara- Processing of BAC Clones. Data from three large insert BAC libraries bidopsis and rice belong to the two major divisions of the plant of maize inbred B73 were used to anchor the DNA sequence to the kingdom, the dicotyledonous and monocotyledonous plants, re- genetic map. The libraries had previously been constructed by spectively. The grass family (Gramineae) is one of the largest partial digestion of genomic DNA with HindIII, EcoRI, and MboI monocotyledonous families; it arose 65 million years ago and is (10, 11), providing a 30-fold physical coverage of the 2.365-Gb comprised of Ͼ10,000 species adapted to one-third of the arable genome (12). land on earth (2). Cereals including rice, sorghum, sugarcane, oat, BAC clones were retrieved from 384-well storage plates and barley, wheat, and maize (corn) are examples of Gramineae species; grown in 96 deep-well plates to saturation. DNAs were extracted they provide a major source of food and feed for humans. with Whatman Unifilters by using a Tomtec liquid handling system. ␮ A significant feature emerging from the genome sequences of DNA precipitates were resuspended in 40 l of buffer; samples of ␮ Arabidopsis and rice is the large number of genes compared to 10 l were used for the forward and reverse sequencing of the BAC ␮ mammalian genomes. Although the gene number in Arabidopsis is ends with universal primers; another 10- l aliquot was used for comparable to that in human and mouse, rice appears to have a DNA fingerprinting. About 75% of the clones were assembled into much larger gene set, due largely to gene amplification (3). Does the a physical map of contiguous, overlapping clones (www.genome. gene number in plants at all correlate to their genome size (4)? Such a question arises, particularly in light of the fact that many crop Freely available online through the PNAS open access option. plants have undergone whole-genome duplication. Maize is an Abbreviations: Gb, gigabase(s); Mb, megabase(s); BAC, bacterial artificial chromosome; interesting example of such a duplication event. In contrast to BES, BAC end sequence; TE, transposable element; GSS, genome survey sequence; TC, wheat, maize has not maintained homoeologous chromosomes, but tentative consensus; HC, high C0t-derived; MF, methyl-filtered; GFS, gene family signature. rather has undergone reassortment of the homoeologous regions Data deposition: The sequences reported in this paper have been deposited in the GenBank acquired from the two progenitor genomes. These regions were first database (accession nos. can be found in Table 4, which is published as supporting demonstrated cytologically between nonhomologous chromosomes information on the PNAS web site). (5) and then later by genetic linkage mapping of nontandem gene †To whom correspondence should be addressed. E-mail: [email protected]. duplicates (6). A comprehensive genetic analysis of homoeologous © 2004 by The National Academy of Sciences of the USA www.pnas.org͞cgi͞doi͞10.1073͞pnas.0406163101 PNAS ͉ October 5, 2004 ͉ vol. 101 ͉ no. 40 ͉ 14349–14354 Downloaded by guest on September 29, 2021 Table 1. Distribution of repetitive DNA in rice and various GSSs of maize as percent of genome Details Total BES HindIII BES EcoRI BES MboI BES UF MF HC RescueMu Rice Total no. of sequences 474,604 309,560 78,313 86,731 50,876 30,000 30,000 30,000 179 Total no. of base pairs 307,169,410 206,221,247 46,673,217 54,274,946 37,621,118 21,649,324 21,637,862 10,074,088 35,800,000 Percent of genome, % 12.99 8.72 1.97 2.29 1.59 0.92 0.91 0.43 8.33 Class I retroelements, % 55.60 58.39 46.77 52.58 57.73 15.70 6.55 4.91 19.28 Ty1͞copia-like elements, % 24.54 25.33 20.54 24.97 17.50 8.37 2.54 1.98 3.67 Ty3͞gypsy-like elements, % 21.43 23.39 15.69 18.94 31.25 4.32 2.22 1.71 8.90 LINES ϩ SINES, % 0.18 0.23 0.06 0.06 0.04 0.06 0.18 0.13 0.96 Other retroelements, % 9.45 9.44 10.48 8.61 8.94 2.95 1.62 1.09 5.74 Class II DNA transposons, % 0.98 0.94 1.16 0.98 0.92 1.14 1.58 4.84 10.35 hAT superfamily, % 0.03 0.02 0.04 0.03 0.04 0.04 0.09 0.11 0.37 CACTA superfamily, % 0.32 0.31 0.38 0.30 0.21 0.21 0.17 0.76 2.83 Mutator, % 0.01 0.01 0.02 0.02 0.01 0.05 0.05 0.36 0.51 MITEs, % 0.17 0.16 0.20 0.17 0.19 0.39 0.62 1.08 3.96 Other DNA transposons, % 0.45 0.42 0.54 0.48 0.48 0.44 0.65 2.53 2.67 Simple repeats, % 0.40 0.27 0.47 0.83 1.66 1.27 0.19 0.17 1.03 High-copy-number genes, % 0.82 0.12 1.13 3.17 1.95 0.17 0.19 0.15 0.06 Other repeats, % 0.12 0.11 0.12 0.16 0.30 0.09 0.06 0.05 0.43 Total repeats, % 57.91 59.82 49.65 57.72 62.55 18.38 8.57 10.13 31.14 Greater than 70% identity limit.
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